Neural precursors exhibit distinctly different patterns of cell migration upon transplantation during either the acute or chronic phase of EAE: A serial MR imaging study

Magnetic Resonance in Medicine

Volumn 65, Issue 6, 2011, Pages 1738-1749

  Muja, Naser ^a   Cohen, Mikhal E ^b   Zhang, Jiangyang ^a   Kim, Heechul ^a   Gilad, Assaf A ^a   Walczak, Piotr ^a   Ben Hur, Tamir ^b   Bulte, Jeff W M ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

blood vessel; cell tracking; multiple sclerosis; neural stem cell; SPIO

Indexed keywords

BLOOD; BLOOD VESSELS; CYTOLOGY; DISEASE CONTROL; IRON OXIDES; MAGNETIC NANOPARTICLES; MAGNETIC RESONANCE IMAGING; MAMMALS; NEUROPHYSIOLOGY;

CELL REPLACEMENT THERAPY; CELL TRACKING; EXPERIMENTAL ALLERGIC ENCEPHALOMYELITIS; MULTIPLE SCLEROSIS; NEURAL STEM CELL; SPATIO-TEMPORAL VARIATION; SPIO; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLES;

STEM CELLS;

BROXURIDINE; SUPERPARAMAGNETIC IRON OXIDE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL TRANSPLANTATION; CONTROLLED STUDY; CORPUS CALLOSUM; FEMALE; GLIOBLASTOMA; MICROGLIA; MOUSE; NEURAL PRECURSOR CELL; NEURAL STEM CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; THREE DIMENSIONAL IMAGING;

EID: 79958287778     PISSN: 07403194     EISSN: 15222594     Source Type: Journal    
DOI: 10.1002/mrm.22757     Document Type: Article

References (43)

1. Trapp BD, Nave KA,. Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci 2008; 31: 247-269.
2. Polman CH, O'Connor PW, Havrdova E, Hutchinson M, Kappos L, Miller DH, Phillips JT, Lublin FD, Giovannoni G, Wajgt A, Toal M, Lynn F, Panzara MA, Sandrock AW,. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med 2006; 354: 899-910.
3. Kappos L, Antel J, Comi G, Montalban X, O'Connor P, Polman CH, Haas T, Korn AA, Karlsson G, Radue EW,. Oral fingolimod (FTY720) for relapsing multiple sclerosis. N Engl J Med 2006; 355: 1124-1140. (Pubitemid 44394919)
4. Miller DH, Soon D, Fernando KT, MacManus DG, Barker GJ, Yousry TA, Fisher E, O'Connor PW, Phillips JT, Polman CH, Kappos L, Hutchinson M, Havrdova E, Lublin FD, Giovannoni G, Wajgt A, Rudick R, Lynn F, Panzara MA, Sandrock AW,. MRI outcomes in a placebo-controlled trial of natalizumab in relapsing MS. Neurology 2007; 68: 1390-1401. (Pubitemid 46659091)
5. Goldschmidt T, Antel J, Konig FB, Bruck W, Kuhlmann T,. Remyelination capacity of the MS brain decreases with disease chronicity. Neurology 2009; 72: 1914-1921.
6. Hauser SL, Oksenberg JR,. The neurobiology of multiple sclerosis: genes, inflammation, and neurodegeneration. Neuron 2006; 52: 61-76. (Pubitemid 44466355)
7. Keirstead HS,. Stem cells for the treatment of myelin loss. Trends Neurosci 2005; 28: 677-683. (Pubitemid 41654392)
8. Muja N, Bulte JWM,. Magnetic resonance imaging of cells in experimental disease models. Prog Nucl Magn Reson Spectros 2009; 55: 61-77.
9. Bulte JW,. In vivo MRI cell tracking: clinical studies. AJR Am J Roentgenol 2009; 193: 314-325.
10. Karussis D, Karageorgiou C, Vaknin-Dembinsky A, Gowda-Kurkalli B, Gomori JM, Kassis I, Bulte JW, Petrou P, Ben-Hur T, Abramsky O, Slavin S,. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 2010; 67: 1187-1194.
11. Aharonowiz M, Einstein O, Fainstein N, Lassmann H, Reubinoff B, Ben-Hur T,. Neuroprotective effect of transplanted human embryonic stem cell-derived neural precursors in an animal model of multiple sclerosis. PLoS One 2008; 3: e3145.
12. Einstein O, Karussis D, Grigoriadis N, Mizrachi-Kol R, Reinhartz E, Abramsky O, Ben-Hur T,. Intraventricular transplantation of neural precursor cell spheres attenuates acute experimental allergic encephalomyelitis. Mol Cell Neurosci 2003; 24: 1074-1082. (Pubitemid 38091518)
13. Einstein O, Grigoriadis N, Mizrachi-Kol R, Reinhartz E, Polyzoidou E, Lavon I, Milonas I, Karussis D, Abramsky O, Ben-Hur T,. Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis. Exp Neurol 2006; 198: 275-284.
14. Einstein O, Fainstein N, Vaknin I, Mizrachi-Kol R, Reihartz E, Grigoriadis N, Lavon I, Baniyash M, Lassmann H, Ben-Hur T,. Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann Neurol 2007; 61: 209-218. (Pubitemid 46557345)
15. Pluchino S, Zanotti L, Rossi B, Brambilla E, Ottoboni L, Salani G, Martinello M, Cattalini A, Bergami A, Furlan R, Comi G, Constantin G, Martino G,. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005; 436: 266-271. (Pubitemid 41021278)
16. Neri M, Maderna C, Cavazzin C, Deidda-Vigoriti V, Politi LS, Scotti G, Marzola P, Sbarbati A, Vescovi AL, Gritti A,. Efficient in vitro labeling of human neural precursor cells with superparamagnetic iron oxide particles: relevance for in vivo cell tracking. Stem Cells 2008; 26: 505-516. (Pubitemid 351413611)
17. Cohen ME, Muja N, Fainstein N, Bulte JW, Ben-Hur T,. Conserved fate and function of ferumoxides-labeled neural precursor cells in vitro and in vivo. J Neurosci Res 2010; 88: 936-944.
18. Bulte JW, Douglas T, Witwer B, Zhang SC, Strable E, Lewis BK, Zywicke H, Miller B, van Gelderen P, Moskowitz BM, Duncan ID, Frank JA,. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol 2001; 19: 1141-1147. (Pubitemid 33115700)
19. Ben-Hur T, van Heeswijk RB, Einstein O, Aharonowiz M, Xue R, Frost EE, Mori S, Reubinoff BE, Bulte JW,. Serial in vivo MR tracking of magnetically labeled neural spheres transplanted in chronic EAE mice. Magn Reson Med 2007; 57: 164-171. (Pubitemid 46067946)
20. Guzman R, Uchida N, Bliss TM, He D, Christopherson KK, Stellwagen D, Capela A, Greve J, Malenka RC, Moseley ME, Palmer TD, Steinberg GK,. Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI. Proc Natl Acad Sci USA 2007; 104: 10211-10216. (Pubitemid 47175288)
21. Alt C, Duvefelt K, Franzen B, Yang Y, Engelhardt B,. Gene and protein expression profiling of the microvascular compartment in experimental autoimmune encephalomyelitis in C57Bl/6 and SJL mice. Brain Pathol 2005; 15: 1-16. (Pubitemid 40224061)
22. Baranzini SE, Bernard CC, Oksenberg JR,. Modular transcriptional activity characterizes the initiation and progression of autoimmune encephalomyelitis. J Immunol 2005; 174: 7412-7422. (Pubitemid 40705713)
23. Ibrahim SM, Mix E, Bottcher T, Koczan D, Gold R, Rolfs A, Thiesen HJ,. Gene expression profiling of the nervous system in murine experimental autoimmune encephalomyelitis. Brain 2001; 124: 1927-1938. (Pubitemid 32945894)
24. Pluchino S, Muzio L, Imitola J, Deleidi M, Alfaro-Cervello C, Salani G, Porcheri C, Brambilla E, Cavasinni F, Bergamaschi A, Garcia-Verdugo JM, Comi G, Khoury SJ, Martino G,. Persistent inflammation alters the function of the endogenous brain stem cell compartment. Brain 2008; 131: 2564-2578.
25. Setzu A, Lathia JD, Zhao C, Wells K, Rao MS, Ffrench-Constant C, Franklin RJ,. Inflammation stimulates myelination by transplanted oligodendrocyte precursor cells. Glia 2006; 54: 297-303. (Pubitemid 44316234)
26. Foote AK, Blakemore WF,. Inflammation stimulates remyelination in areas of chronic demyelination. Brain 2005; 128: 528-539. (Pubitemid 40380188)
27. Aarum J, Sandberg K, Haeberlein SL, Persson MA,. Migration and differentiation of neural precursor cells can be directed by microglia. Proc Natl Acad Sci USA 2003; 100: 15983-15988. (Pubitemid 38021101)
28. Neumann H, Kotter MR, Franklin RJ,. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 2009; 132: 288-295.
29. Kotter MR, Setzu A, Sim FJ, Van Rooijen N, Franklin RJ,. Macrophage depletion impairs oligodendrocyte remyelination following lysolecithin-induced demyelination. Glia 2001; 35: 204-212. (Pubitemid 32827763)
30. Ben-Hur T, Einstein O, Mizrachi-Kol R, Ben-Menachem O, Reinhartz E, Karussis D, Abramsky O,. Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis. Glia 2003; 41: 73-80. (Pubitemid 36164286)
31. Bulte JW, Ben-Hur T, Miller BR, Mizrachi-Kol R, Einstein O, Reinhartz E, Zywicke HA, Douglas T, Frank JA,. MR microscopy of magnetically labeled neurospheres transplanted into the Lewis EAE rat brain. Magn Reson Med 2003; 50: 201-205. (Pubitemid 36841877)
32. Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D, Lira S, Uccelli A, Lanzavecchia A, Engelhardt B, Sallusto F,. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat Immunol 2009; 10: 514-523.
33. Bartholomaus I, Kawakami N, Odoardi F, Schlager C, Miljkovic D, Ellwart JW, Klinkert WE, Flugel-Koch C, Issekutz TB, Wekerle H, Flugel A,. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 2009; 462: 94-98.
34. Owens T, Bechmann I, Engelhardt B,. Perivascular spaces and the two steps to neuroinflammation. J Neuropathol Exp Neurol 2008; 67: 1113-1121.
35. Sellers DL, Maris DO, Horner PJ,. Postinjury niches induce temporal shifts in progenitor fates to direct lesion repair after spinal cord injury. J Neurosci 2009; 29: 6722-6733.
36. Stubbs D, DeProto J, Nie K, Englund C, Mahmud I, Hevner R, Molnar Z,. Neurovascular congruence during cerebral cortical development. Cereb Cortex 2009; 19 (suppl 1): i32-i41.
37. Palmer TD, Willhoite AR, Gage FH,. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000; 425: 479-494.
38. Chintawar S, Cayrol R, Antel J, Pandolfo M, Prat A,. Blood-brain barrier promotes differentiation of human fetal neural precursor cells. Stem Cells 2009; 27: 838-846.
39. Roscoe WA, Welsh ME, Carter DE, Karlik SJ,. VEGF and angiogenesis in acute and chronic MOG(s35-55) peptide induced EAE. J Neuroimmunol 2009; 209: 6-15.
40. Ohab JJ, Carmichael ST,. Poststroke neurogenesis: emerging principles of migration and localization of immature neurons. Neuroscientist 2008; 14: 369-380. (Pubitemid 352010071)
41. Wuerfel J, Haertle M, Waiczies H, Tysiak E, Bechmann I, Wernecke KD, Zipp F, Paul F,. Perivascular spaces-MRI marker of inflammatory activity in the brain? Brain 2008; 131: 2332-2340.
42. Tonra JR, Reiseter BS, Kolbeck R, Nagashima K, Robertson R, Keyt B, Lindsay RM,. Comparison of the timing of acute blood-brain barrier breakdown to rabbit immunoglobulin G in the cerebellum and spinal cord of mice with experimental autoimmune encephalomyelitis. J Comp Neurol 2001; 430: 131-144.
43. Brown DA, Sawchenko PE,. Time course and distribution of inflammatory and neurodegenerative events suggest structural bases for the pathogenesis of experimental autoimmune encephalomyelitis. J Comp Neurol 2007; 502: 236-260. (Pubitemid 46595397)